Recombination-aware phylogenomics unravels the complex divergence of hybridizing species.

Abstract

Current phylogenomic approaches implicitly assume that the predominant phylogenetic signal within a genome reflects the true evolutionary history of organisms, without assessing the confounding effects of gene flow that result in a mosaic of phylogenetic signals that interact with recombinational variation. Here we tested the validity of this assumption with a recombination-aware analysis of whole genome sequences from 27 species of the cat family. We found that the prevailing phylogenetic signal within the autosomes is not always representative of speciation history, due to ancient hybridization throughout felid evolution. Instead, phylogenetic signal was concentrated within large, conserved X-chromosome recombination deserts that exhibited recurrent patterns of strong genetic differentiation and selective sweeps across mammalian orders. By contrast, regions of high recombination were enriched for signatures of ancient gene flow, and these sequences inflated crown-lineage divergence times by ~40%. We conclude that standard phylogenomic approaches to infer the Tree of Life may be highly misleading without considering the genomic partitioning of phylogenetic signal relative to recombination rate, and its interplay with historical hybridization.